- A common symbiotic region was wholly conserved within the Rhizobium genus yet different from those of the other two genera. - Among the six putative novel species exclusive to China, horizontal transfer of symbiosis genes suggested symbiosis with other indigenous legumes and loss of originally symbiotic regions or non-symbionts before the introduction of common bean into China. - Genome data for Ensifer and Bradyrhizobium strains indicated symbiotic compatibility between microsymbionts of common bean and other hosts such as soybean.. - 2020 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0. - Full list of author information is available at the end of the article. - Like many other legumes, common bean plants form efficient nitrogen-fixing nodules with diverse rhizobia [5–7]. - To date, 18 Rhizobium species have been isolated from common bean root nodules. - americanum [10] can nodulate common bean plants in alkaline-saline soils. - Some of these rhizobia have been detected in both the centers of origin and other areas because they can be introduced with common bean seeds [11].. - Common bean is believed to have been introduced into China directly from Latin America around 400 years ago [12], and China is now one of the world’s major pro- ducers of common bean. - In previous studies, 371 rhizo- bial strains were isolated from root nodules of common bean plants grown in fields at 21 sample sites in four provinces in China [13, 14]. - Some of these common bean-nodulating rhizobia were also found in association with other hosts, such as Vicia faba (fava bean) and Trifolium spp. - How such an extraordinary variety of genotypes from three distinct genera (Rhizobium, Bradyrhizobium, and Ensi- fer) evolved into microsymbionts of common bean after its introduction into China is very interesting.. - However, it is unclear whether common bean enhances HGT in rhizobia during its adaptation to the introduced environment. - Furthermore, common bean and Glycine max L. - Therefore, the relationships of symbiosis genes in Ensifer and Bradyrhizobium strains that nodu- late common bean and soybean in China are of interest.. - Common bean belongs to the secondary category even though three ge- notypes of rhizobial symbiosis genes (sv. - To clarify how different rhizobial species were re- cruited as symbionts of common bean in China, com- parison of individual symbiosis genes, such as nodC, could provide insight into the phylogenetic relationships [40]. - Fortunately, genomics has revolutionized the way for estimation of the phylo- genetic relationships among microbes, including the. - Herein, we chose 25 representatives of common bean -nodulating rhizobia from China (19 Rhizobium, two Ensifer, and four Bradyrhizobium), and four from Mexico (two Rhizobium and two Ensifer), for compara- tive genomics analysis with reference strains. - To analyze genomic features among strains in the Rhizo- bium genus occupying diverse niches, we used the 50 available Rhizobium genomes (Additional file 1: Table S1) to probe the evolution of the gene repertoire through pan-genome analysis. - The core genome represented 39.93 to 47.59% of the repertoire of protein-coding genes in each strain. - The hierarchical cluster derived from these data clearly distinguished strains of the same spe- cies from those of different species (Fig. - b Hierarchical clustering of Rhizobium genomes based on a heatmap of 30,767 genes in the pan-genome. - The presence and absence of the 30,767 genes are indicated by bisque and azure, respectively. - The Shimodaira–Hasegawa test for the comparison between the phylogenetic tree for each of the 2654 core genes and the species tree uncov- ered 191 genes with consistent phylogenies (Add- itional file 1: Table S2). - These 16 genes may perform essential biological functions in the survival of rhizobial strains. - To investigate HGT events in the Rhizobium genus, we obtained the complete sequences of symbiosis plasmids from R. - Most of the nod, nif, and fix symbiosis genes were clustered in a 0.1 Mb region on symbiosis plasmid pRapFH23a (Additional file 2: Figure S4).. - nearly identical among most of the HGT events between two species (Fig. - In addition, most of the HGT genes were found on symbiosis plasmids, and on accessory plasmid p42a in strains R4 and R17 (R4-CFN4 and R17-FH14. - encoding plasmid proteins with key functions such as (1) replication (e.g., the repABC operon) and (2) conju- gation (e.g., type IV secretion system and conjugative transfer relaxase). - a Comparison of the predicted number of recent HGT genes and the number of highly conserved plasmid genes between the reference genome of R4-CFN42 (R. - b Genomic locations of the predicted HGT genes between R4-CFN42 and other sample strains. - c All HGT events in the tested Rhizobium strains.. - To explore the phylogenetic relationship of symbiosis plasmids in the two HGT groups, we constructed a bipartite ‘gene families-plasmids’ network of 13 symbiosis plasmids from the Rhizobium strains nodulating P. - Relationships between microsymbionts of common bean and other hosts. - Among the eight sequenced common bean micro- symbionts, all four Ensifer strains and two Bradyrhizo- bium strains (Y21 and L2) displayed close relationships with soybean microsymbionts, while the other two Bra- dyrhizobium strains (C9 and Y36) exhibited unique gen- ome content (Additional file 1: Table S4). - Unlike the Rhizobium strains, these common bean microsymbionts only shared HGT genes with the microsymbionts of other legume species, such as Glycine. - 3 Genome comparison of Ensifer and Bradyrhizobium mostly isolated from common bean and soybean. - We also analyzed 12 critical genes related to nodulation and nitrogen fixation (nodABC, fixABC, and nifHDKENB) in the eight common bean microsymbionts. - III FG01 and NG07B, iso- lated from root nodules of common bean in Mexico, shared almost identical nodulation- and nitrogen fixation- related genes, and these genes differed from those in Ensi- fer sp. - Cross-nodulation tests further verified that strains PCH1, CCBAU83753, and CCBAU05631 could effectively nodu- late common bean and soybean.. - Nodulation gene extraction failed for strain Y36, consistent with its inabil- ity to nodulate with common bean or occasional forma- tion of rod-like and whites nodules. - Cross-nodulation tests revealed that both C9 and CCBAU43297 could effectively nodulate common bean and soybean while Y21, CCBAU41267, and CCBAU15615 formed white nodules with common bean and pink nodules with soybean. - Strains Y21 and C9 isolated from nodules of common bean might be soybean micro- symbionts. - Their isolation from common bean indicates that this legume species can act as a promiscuous host.. - In this study, we sequenced rhizobial genomes from 29 common bean microsymbionts in three distinct genera,. - The trends of the first two categories (I and Q) are consistent with the genome analysis results of soybean microsymbionts (Ensifer and Bradyrhizobium strains) [41]. - The result of the third category (V) supports an earlier study on gene content in the genomes of 115 prokaryotic species [46].. - Pan-genome analysis is an efficient tool for revealing the diversity and composition of the gene repertoire [48].. - The 50 Rhizobium strains were divided into 19 taxonomic clusters, with a shared core genome that represented less than half of the repertoire of protein- coding genes in each strain. - Of note, strains in the same cluster, des- pite isolated from diverse environments (countries or hosts), were more inclined to recruit lineage-specific shell genes under direct or indirect control through the speci- ation process, based on hierarchical clustering of the pan- genome. - Apart from five core genes, most of the species-related genes were detected on chromosomes. - Based on comparison of the genomes of 50 Rhizobium strains, we assigned the 19 sequenced Chinese common bean microsymbionts to four defined species (R. - anhuiense may be the dominant common bean micro- symbiont in China, despite the reference strain of R.. - In the phylogenies of 12 symbiosis genes (Additional file 2:. - Thus, common bean microsymbionts might be microsym- bionts of other indigenous legumes before the introduction of common bean into China. - Herein, we present strong evidence that indigenous Rhizobium strains likely acquired their common bean-specific symbiosis genes from other Rhizobium species that were introduced alongside bean crops.. - Comparative genomic analysis and cross-nodulation tests of Ensifer and Bradyrhizobium strains indicated symbiotic compatibility between soybean microsym- bionts and common bean microsymbionts. - This raises an interesting question: were non-symbiont strains driven to obtained “new skill” in the soil by themselves or in the nodules by plants or by other factors? Here we found that symbiosis genes in the Rhizobium genus belong to a phylogenetically compact group, although common bean can be nodulated by rhizobia from distinct genera. - Among the 19 sequenced Chinese common bean micro- symbionts, strains of R. - anhuiense and six putative novel Rhizobium species are exclusive to China, and they appear to have evolved into common bean microsymbionts via HGT events with Mexican rhizobia after being introduced into China. - Common bean- nodulating Ensifer and Bradyrhizobium strains possess symbiotic regions distinct from those in Rhizobium strains, indicating symbiotic compatibility between microsymbionts of soybean and common bean. - We chose a total of 29 common bean microsymbionts (21 Rhizobium, four Ensifer, and four Bradyrhizobium), including 25 from China and four from Mexico. - Other reference genomes used in the study included 29 Rhizo- bium strains (17 Phaseolus vulgaris microsymbionts, eight Trifolium spp. - The draft genomes of 29 common bean microsymbionts were obtained as previously described [15] using the Illumina HiSeq platform at Novogene (Beijing, China).. - genomes of 29 common bean microsymbionts and the complete genome of R. - acidisoli FH23 have been depos- ited in the GenBank database under project accession no. - water-agar plates in the dark [72]. - Each bag was inocu- lated with 1 mL of the 24 to 72 h culture of rhizobial strains, in triplicate. - Bipartite analysis of the symbiosis plasmids. - Visualization of the network was performed using Gephi’s built-in For- ceAtlas2 algorithm with default parameters, except for the following: approximate speed = 1.0, scaling = 200, gravity = 1.0, and ‘prevent overlap’.. - Graphical circular map of the complete genome of R. - The outermost circle represents the coordi- nates of the genome sequence. - The darker the link color, the lar- ger the predicted magnitude of the recent HGT event. - Corre- logram showing correlations between genome size, protein-coding sequences, and COG assignments of the 29 rhizobial strains in three dis- tinct genera. - The darker and more saturated the color, the greater the magnitude of the correlation. - The draft genomes of 29 common bean microsymbionts and the complete genome of R. - acidisoli FH23 have been deposited in the GenBank database under project accession no. - An earth-system perspective of the global nitrogen cycle. - Diversity in the rhizobia associated with Phaseolus vulgaris L. - Genetic diversity of indigenous common bean (Phaseolus vulgaris) rhizobia in two Brazilian ecosystems. - fixes nitrogen with common bean (Phaseolus vulgaris L.) in a northern Tunisian field. - Nitrogen-fixing rhizobial strains isolated from common bean seeds:. - Genetic diversity of Chinese common bean (Phaseolus vulgaris L.) landraces assessed with simple sequence repeat markers. - Biodiversity and biogeography of rhizobia associated with common bean (Phaseolus vulgaris L.) in Shaanxi Province. - Population genomics of the symbiotic plasmids of sympatric nitrogen- fixing Rhizobium species associated with Phaseolus vulgaris. - The composite genome of the legume symbiont Sinorhizobium meliloti. - Genome sequence of Bradyrhizobium japonicum E109, one of the most agronomically used nitrogen-fixing rhizobacteria in Argentina. - Biserrulae strain WSM1284, an efficient nitrogen-fixing microsymbiont of the pasture legume Biserrula pelecinus. - Biodiversity and biogeography of rhizobia associated with soybean plants grown in the North China plain. - Rhizobial diversity and nodulation characteristics of the extremely promiscuous legume Sophora flavescens. - Nodulation of legumes by members of the beta-subclass of Proteobacteria. - Transcriptomic studies of the effect of nod gene-inducing molecules in rhizobia: different weapons, one purpose.. - Symbiosis specificity in the legume:. - A genomotaxonomy view of the Bradyrhizobium genus. - Angiuoli SV, et al structure and dynamics of the pan-genome of Streptococcus pneumoniae and closely related species. - Comparative genomic analysis of N 2 -fixing and non-N 2 -fixing Paenibacillus spp.: organization, evolution and expression of the nitrogen fixation genes. - New insights into the origins and evolution of rhizobia that nodulate common bean (Phaseolus vulgaris) in Brazil
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